H. ÖZBEK, S. ÇORUH

Turk J Zool 2012; 36(4): 447-459 © TÜBİTAK Research Article doi:10.3906/zoo-1104-12

Larval and larval diseases of neustria L. (: ) detected in Erzurum Province,

Hikmet ÖZBEK*, Saliha ÇORUH Department of Plant Protection, Faculty of Agriculture, Atatürk University, Erzurum - TURKEY

Received: 12.04.2011

Abstract: Th e larval parasitoids and larval diseases of Malacosoma neustria (L.) (Lepidoptera: Lasiocampidae) in various host plants were investigated in Erzurum Province, Turkey, during 2004 and 2005. Th e larval parasitoids were reared in a laboratory, and a total of 29 were established in association with the larvae of M. neustria in the families (Diptera), Braconidae, , and Chalcidoidea (). Of the 6 tachinid parasitoids, Pales pavida (Meigen) was the most prevalent species and accounted for 25% of the tachinid records. Among the tachinids, there were 2 new records for the Turkish fauna: Exorista amoena Mesnil and Palesisa nudioculata Villeneuve. Exorista amoena was reared from M. neustria for the fi rst time. Th e braconid species Meteorus lionotus Th omson and Cotesia vanessa (Reinhard) were also reared from M. neustria for the fi rst time. Among the 10 chalcidoid species reared, Monodontomerus aereus Walker and Brachymeria secundaria (Rusc.) were the most prevalent species. Five chalcidoid species, Asaphes suspensus (Nees), A. vulgaris Walker (), Brachymeria secundaria (Ruschka) (), Eupelmus urozonus Dalman (), and Eurytoma verticillata (F.) (), were reared from M. neustria for the fi rst time. Of the 10 species of ichneumonids reared, Exeristes roborator F. was the most abundant and accounted for 35% of the total ichneumonid records. Th e total parasitism rate of all parasitoids was 33.7%. As disease agents of M. neustria, the nuclear polyhedrosis virus and 4 pathogenic bacteria, Brevibacillus agri, Alcaligenes xylosoxydans xylosoxydans (Achromobacter xylosoxidans), Bacillus lentimorbus, and Serratia fonticola, were diagnosed. All of the bacteria from M. neustria were recorded for the fi rst time. Th e percentage of diseased larvae was low, about 3%.

Key words: Lepidoptera, Lasiocampidae, Malacosoma neustria, parasitoids, disease, bacteria, virus, Erzurum, Turkey

Erzurum İli’nde (Türkiye) Malacosoma neustria L. (Lasiocampidae: Lepidoptera)’nın parazitoitleri ve hastalıkları

Özet: Değişik konukçularda beslenen Malacosoma neustria (L.) (Yüzükkelebeği) (Lepidoptera: Lasiocampidae)’nın larva parazitoitleri ve larva hastalıkları 2004 ve 2005 yıllarında Erzurum İli’nde araştırılmıştır. Laboratuar koşullarında, Tachinidae (Diptera), Braconidae, Ichneumonidae ve Chalcidoidae (Hymenoptera)’ye ait toplam 29 parazitoid türü elde edilmiştir. Saptanan altı tachinid türünden Pales pavida (Meigen) ve Tachina praeceps Meigen en fazla yoğunluk oluşturmuşlardır. Exorista amoena Mesnil ve Palesisa nudioculata Villeneuve Türkiye faunası için yeni türlerdir. Exorista amoena ilk defa bu çalışma ile M. neustria’dan elde edilmiştir. İki braconid türü olan Meteorus lionotus Th omson ve

* E-mail: [email protected]

447 Larval parasitoids and larval diseases of Malacosoma neustria L. (Lepidoptera: Lasiocampidae) detected in Erzurum Province, Turkey

Cotesia vanessa (Reinhard)’nın M. neustria larvalarını parazitlediği ilk defa belirlenmiştir. Topam 10 chalcidoid türü arasında, Monodontomerus aereus Walker ve Brachymeria secundaria (Rusc.) en yaygın olanlardır ve tüm chalcidoidlerin sırasıyla % 35 ve % 32’ini oluşturmaktadırlar. Asaphes suspensus (Nees), A. vulgaris Walker (Pteromalidae), Brachymeria secundaria (Ruschka) (Chalcididae), Eupelmus urozonus Dalman (Eupelmidae) ve Eurytoma verticillata (F.) (Eurytomidae) türleri ilk kez M. neustria’dan elde edilmiştir. Tolam 10 tür olan ichneumonidler içerisinde, Exeristes roborator F. en yaygın olanıdır ve ichneumonidlerin % 35’ini oluşturmaktadır. Tüm parazitoitlerin toplam parazitleme oranı % 33,7 olarak belirlenmiştir. M. neustria larvalrında hastalık etmeni olarak nükleer polyhedrosis virüsü (NPD) ve Brevibacillus agri, Alcaligenes xylosoxydans xylosoxydans (Achromobacter xylosoxidans), Bacillus lentimorbus ve Serratia fonticola olmak üzere dört bakteri türü, tespit edilmiştir. Bu türler, M. neustria’dan ilk defa elde edilmişlerdir. Hastalıklara bağlı olarak saptanan larvalardaki ölüm oranı yaklaşık % 3 düzeyindedir.

Anahtar sözcükler: Lepidoptera, Lasiocampidae, Malacosoma neustria, parasitoitler, hastalıklar, bakteri, virüs, Erzurum, Türkiye

Introduction more abundant and destructive, particularly in sea Th e European tent or lackey , buckthorn, barberry, and some rose species (Çoruh Malacosoma neustria (L.) (Lepidoptera: and Özbek, 2002). Lasiocampidae), known as “yüzükkelebeği” or M. neustria is univoltine and overwinters in the “yüksükkelebeği” in Turkish, is one of the most form of egg masses on twigs of the host plants. Newly widely distributed species, particularly in the eastern emerged larvae crawl to the crown, feed gregariously, and central Anatolian parts of Turkey (İren, 1977; and gather at major branch forks to construct Çoruh and Özbek, 2002). Its distribution range in the webbing (tents), which are white in color and easily world is wide: Europe, northern Africa, Iran, Syria, recognized. Larvae () feed both in the tent Siberia, China, Mongolia, Taiwan, North Korea, and as well as outside the crown. As the larvae develop, Japan (Dobesberger, 2002). It has been recognized they become solitary and eventually seek sheltered as an important defoliator of a wide variety of locations to pupate. Th e cocoons are yellowish-white, deciduous hardwood trees and shrubs throughout loose, and usually occur in clusters (Çoruh and its range for many years (Bodenheimer, 1958; İren, Özbek, 2002). 1977; Çanakçıoğlu and Mol, 1998; Özbek et al., 1998; Populations of M. neustria periodically attain Çoruh and Özbek, 2002; Özbek and Çalmaşur, 2005). outbreak proportions in eastern Anatolia. During Malacosoma species are widespread and are outbreaks, a large number of caterpillars cause important defoliators of various types of cultivated widespread and extensive defoliation of host plants and wild plants (Costa, 1997). M. neustria has a and may create an overwhelming nuisance to people wide host range that includes many fruit trees such encountering them. Severe and repeated defoliation as (Malus communis L.), (Pyrus communis can lead to dieback and/or reduced growth in the L.), (Prunus spp.), and mulberry (Morus aff ected plants, which in some instances may be sp.), and wild and ornamental trees and shrubs serious. Although the outbreak periods reported are including (Quercus spp.), rose (Rosa spp.), irregular, since 1970 the outbreaks have been reported oleaster (Elaeagnus angustifolia L.), sea buckthorn at 3-7 year intervals in the province of Erzurum. (Hippophae rhamnoides L.), barberry (Berberis Following several consecutive years of defoliation spp.), and elm (Ulmus spp.). Other deciduous trees in any locality, leaves of the susceptible host plants, and shrubs such as (Salix spp.), poplar and especially Rosa canina L., Berberis vulgaris L., and aspen (Populus spp.), birch (Betula spp.), ash tree Hippophae rhamnoides L., were completely defoliated (Fraxinus spp.), currant (Ribes spp.), and bramble and the damaged twigs were very oft en dry. At bushes (Rubus spp.) are also damaged occasionally times, the whole plant dries up (Çoruh and Özbek, (Bodenheimer, 1958; İren, 1977; Özbek et al., 1998; 2002). Traditionally, fruits of these plants have been Çoruh and Özbek, 2002; Özbek and Çalmaşur, 2005; consumed by people living in rural areas. However, in Özbek and Çoruh, 2010). In eastern Anatolia it is recent years, these plants have attracted considerable

448 H. ÖZBEK, S. ÇORUH

international attention from horticulturists, Çoruh (2010) recorded egg parasitoids of M. neustria biochemists, and pharmacologists because of the in Erzurum Province. Although some researchers fragrance of the fl owers (Rosa spp.) and the high have obtained various parasitoid species in the content of biologically active substances in their fruits families Tachinidae (Diptera) and Ichneumonidae and other organs, such as vitamin C, carotenoids, (Hymenoptera) from larvae of M. neustria during fl avonoids, minerals, and certain enzymes, as well their parasitoidal studies on various groups of as vitamins B1, B2, E, and K. Th e above mentioned (Doğanlar, 1975; Uğur, 1985; Kansu et al., 1986; plant species are increasingly important because of Özdemir and Kılınçer, 1990), there has been no in- this high antioxidant capacity (Li and Schroeder, depth study of the larval parasitoids of M. neustria 1996; Küpeli et al., 2002; Melnicova et al., 2002; in Turkey. Demir, 2005a , 2005b; Tiitinen et al., 2005; Ercişli et al., 2007; Özbek, 2009). It would also be worthwhile Th e objectives of the present study were to to mention that these plants may be very valuable for determine the identities of the parasitoids and disease promoting wildlife, especially in their native range agents attacking larvae of M. neustria in Erzurum where many use their leaves and fruits for Province, Turkey; to determine natural parasitism food and shelter. rates; and to show the potential of parasitoid(s) and disease agent(s) for classical biological control of M. Climatic conditions, natural enemies, and other neustria in Turkey or other countries suff ering from factors have been considered in ending outbreaks of this pest. insects. Parry (1995) pointed out that elevated levels of parasitism were oft en associated with the collapse An outbreak of M. neustria was observed in 2002, of outbreaks. Mirchev et al. (2001) emphasized that which lasted for about 5 years. Th e present study was parasitoids play an important role in reducing the conducted during this outbreak period. population density of many forest pests. Despite its importance as a pest on various trees Materials and methods and shrubs, studies of the natural enemies of M. neustria in Turkey are very limited. Bulut (1991) Collection sites studied egg parasitoids of this species in Ankara and Field studies were conducted during 2004 and 2005 neighboring provinces. More recently, Özbek and at 3 sites (Figure).

İstanul

Ankara Erzurum Aegean Sea

Mediterranean Sea 3 1 . University Campus 2 2 . Tortum 3 . Oltu 1

Figure. Sampling sites of larval parasitoids of Malacosoma neustria L. in Erzurum Province, Turkey.

449 Larval parasitoids and larval diseases of Malacosoma neustria L. (Lepidoptera: Lasiocampidae) detected in Erzurum Province, Turkey

Th e fi rst collection site was the campus of Atatürk Sampling and rearing University in Erzurum, which has more than 800 To obtain parasitoids, the larvae (caterpillars) were ha of wooded area and grass lands at an altitude of collected from the sites. Two samples were collected in 1850 m. Although the trees were predominantly each season during 2004 and 2005. Th e fi rst sampling Pinus sp., there were various deciduous trees and was done in the fi rst week of June and predominantly bushes; the most abundant hosts among them were comprised second and third instar larvae. Th e second Rosa canina L. (Rosaceae), Elaeagnus angustifolia sampling, which was done during the second week of L. (Elaeagnaceae), and Betula verrucosa (Youngii) June, consisted of fourth and fi ft h instar larvae. Th e (Betulaceae). Elaeagnus angustifolia was rare and larvae were picked up along with shoots and leaves of occurred sporadically. Th e second collection site was randomly chosen host plants. Th ese were placed into about 80 km northeast of Erzurum in the village of labeled cotton bags and brought to the laboratory. Th e Aksu (Tortum District), which could be characterized larvae were transferred to fi ne-mesh nylon rearing as hilly, uncultivated land ranging from 1950 to 2000 cages (30 × 30 × 50 cm). Th e shoots and leaves of the m in altitude. Common barberry, B. vulgaris, and R. host plants were dipped into a glass container fi lled canina, the most abundant host plants, were scattered with water and covered with a cotton stopper. Th e among various species of shrubs and ; common containers were kept in a rearing room at 25 ± 2 °C barberry was the most predominant host plant. Th e and 60%-70% relative humidity with natural light. third collection site was about 110 km northeast of Periodically, withered shoots and leaves were renewed Erzurum, between Çamlıbel and Sarısaz villages (Oltu with fresh ones. Soil of about 2 cm in depth was added District), with cultivated land at about 1300-1400 m. to the bottom of the cage to facilitate pupation of the Two preferred hosts, sea buckthorn (H. rhamnoides) parasitoids. Th e rearing cages were checked daily and and wild plum (Prunus sp.), were abundant and the pupae and/or cocoons of the parasitoids were mixed with various species of deciduous trees and transferred to petri dishes (1.5 × 9 cm). Emerging shrubs along the borders of fi elds. Potatoes were adults of parasitoids in the cages and petri dishes were cultivated in small areas with rare application of removed, killed, and prepared for identifi cation. Th e insecticides, and thus the adverse eff ect of chemicals percentage of parasitism was calculated by dividing the was negligible. Th e purpose of choosing 3 locations number of larvae out of which parasitoids emerged by with diff erent habitats was to increase the chance of the total number of larvae in a sample. diversity among the parasitoids obtained. To obtain microorganisms, sluggish or exhausted At the third collection site (Oltu), as Doğanlar (unhealthy looking) larvae on the foliage and in the (1982b) indicated, another Malacosoma species, M. tents of M. neustria were collected, inserted into franconica Denis & Schiff ermuller, was present in sterilized tubes to prevent possible contamination, addition to M. neustria. Although it was possible and brought to the laboratory. All of the isolated to distinguish the 2 species from their larvae, it was bacterial strains were identifi ed based on fatty easier to identify them from the egg masses. Both acid methyl ester (FAME) profi les using Sherlock of the species showed similar egg-laying habits and Microbial Identifi cation System soft ware (Microbial placed their eggs as masses around small twigs or ID, Newark, DE, USA). Nuclear polyhedrosis virus branches of the host plants. However, the egg masses (NPV) was observed by killing larvae in the fi eld. of M. franconica were covered with a mass of light NPV was identifi ed under a normal light microscope gray substance that had the appearance of a hardened, by the presence of occlusion bodies. stiff , shiny cover. Th e egg masses of M. neustria were Identifi cation of the parasitoids was verifi ed naked and uncovered. Th e eggs could be counted even by comparison with the preserved specimens with the naked eye. Th erefore, it was easy to separate in the Entomology Museum, Erzurum, Turkey. the egg masses of these 2 Malacosoma species in the Th e unidentifi ed specimens were determined by fi eld. From the egg masses near tents, the larvae or specialists. Th e adults of parasitoids were deposited tents of M. neustria could be recognized. It was also in the EMET. Among the bacteria, isolation and noted that M. franconica was not as abundant as M. determination of Brevibacillus agri was made by neustria in the research area. Fikrettin Şahin, and the rest by Arzu Ala Görmez.

450 H. ÖZBEK, S. ÇORUH

Results and discussion In Tachinidae, 3 species of Exorista were reared A total of 29 species of parasitoids were reared from from larvae of M. neustria from the fi rst collection the larvae of M. neustria during 2004 and 2005 (Table site (university campus): E. segregata (Rondani), E. 1). Among the parasitoids, 6 species in Tachinidae amoena Mesnil, and E. larvarum (L.). Among them, (Diptera), 2 species in Braconidae (Hymenoptera), E. segregata was the most abundant species; it fi rst and 10 species each in Chalcidoidea (Hymenoptera) emerged on 23 July and continued for the next 5 days. and Ichneumonidae (Hymenoptera) were reared. Th e Exorista segregata was previously reared from the composition of parasitoid species was more diverse larvae of M. castrensis kirghisica Staudinger and M. at the fi rst collection site than at the second or third. franconica Denis & Schiff ermuller in Erzurum Province

Table 1. Larval parasitoids of Malacosoma neustria L. in Erzurum Province, Turkey, reared during 2004 and 2005.

Locations Family and order Parasitoid species First collection Second collection Th ird collection site, A.U. campus site, Tortum site, Oltu Exorista amoena Mesnil + E. larvarum L. + E. segregata Rond. + Tachinidae (Diptera) Masicera sphingivora (R.D.) + + Pales pavida Meig. + + Palesisa nudioculata Vill. + Tachina praeceps Meig. + + Meteorus lionotus Th omson + Braconidae (Hymenoptera) Cotesia vanessa (Reinhard) + Asaphes suspensus (Nees) + A. vulgaris Walker + Brachymeria secundaria (Rusc.) + Eupelmus urozonus Dalman + Eurytoma verticillata (F.) + Chalcidoidea (Hymenoptera) Monodontomerus aereus Walker + Pediobius bruchicida Rondani + Pronotalia carlinarum (Sz. & Er.) + Psychophagus omnivorus (Walker) + Torymus triangularis Th omson + Endromopoda phragmitidis P. + Exeristes roborator F.+++ Gregopimpla inquisitor (Scop.) + G. malacosomae (Sey.) + Itoplectis viduata Grav. + Ichneumonidae (Hymenoptera) Lysibia nana (Grav.) + Pimpla turionellae L. + + P. r ufi pes Brulle + + Scambus nigricans (Th om.) + Tromatobia ornata (Grav.) +

451 Larval parasitoids and larval diseases of Malacosoma neustria L. (Lepidoptera: Lasiocampidae) detected in Erzurum Province, Turkey

(Doğanlar, 1982a). Additionally, parasitoids of various reared this species from the larvae of M. castrensis in species in the lepidopteran families Lymantriidae, Erzurum Province. It is reasonable to believe that this Noctuidae, Notodontidae, Nymphalidae, Pieridae, species was fi rst reared from M. neustria in Turkey. Sphingidae, Th aumetopoeidae, and Zygaenidae were Kara and Tschorsnig (2003) listed Malacosoma noted (Kara and Tschorsnig, 2003). Exorista amoena alpicola Staudinger and Euproctis chrysorrhoea was reared from M. neustria for the fi rst time in the (L.) (Lepidoptera: Lymantriidae) as other hosts present study and was added as a new record for the of T. praeceps. Among the tachinid parasitoids, P. Turkish fauna. Th e adults fi rst emerged on 26 July pavida, T. praeceps, and P. nudioculata were the most and continued for the next 3 days. prevalent species, accounting for 25%, 21%, and 20% fi rst emerged on 26 July and continued for about 1 of the records, respectively. week. It was known as a parasitoid of M. neustria, In addition to species mentioned above, Doğanlar and it parasitized M. castrensis kirghisica and (1975) obtained 2 tachinid species, Drino imberbis various lepidopteran species belonging to families Wiedeman and D. inconspicua Meigen, from the Arctiidae, Lymantriidae, Noctuidae, Pieridae, and larvae of M. neustria in Erzurum Province. Kansu et

Pyralidae (Kara and Tschorsnig, 2003). Th e larvae al. (1986) recorded Compsilura concinnata (Meigen) of the 3 Exorista species emerging from the host from the larvae of M. neustria in central Anatolia. pupated in the soil at the base of the cage. Masicera Additionally, Doğanlar (1982b) obtained Eucarcelia sphingivora (Robineau-Desvoidy) was recorded from separate (Rondani), atripalpis Rob.-Des., the university campus and Tortum. Th e adults fi rst and Rob.-Des. from the larvae of emerged on 27 July and continued until 11 August. M. castrensis in Erzurum Province. Th ese 3 tachinid It was known as a parasitoid of M. neustria, and it species were reported as parasitoids of M. neustria attacked several lepidopteran species belonging to the (Mesnil, 1965; Kara and Tschorsnig, 2003). Although families Sphingidae, Lymantriidae, and Noctuidae Doğanlar (1975) obtained Histochaeta marmorata (Kara and Tschor snig, 2003). Pales pavida (Meigen) Fabricius from Arctia caja (L.) (Lepidoptera: was found on the university campus and in Tortum. Arctiidae) in Erzurum, this species is also known Th e adults emerged from the host pupae from 22 July as a parasitoid of M. neustria (Emden, 1954). From to 9 August. It also parasitized M. castrensis kirghisica all these reports, we can conclude that 11 or more and M. franconica (Doğanlar, 1982b). Recently, tachinid species could parasitize the larvae of M. Özbek and Çalmaşur (2010) obtained P. pavida from neustria in Erzurum Province as well as other the pupae of pantaria (L.) (Lepidoptera: locations in Turkey. Geometridae) in November in eastern Anatolia, Turkey. Belshaw (1993) listed 39 lepidopteran species Parasitoid species in the family Braconidae (2 as hosts of P. pavida. Palesisa nudioculata Villeneuve braconid species), Meteorus lionotus Th omson was reared from the larvae of M. neustria from the and Cotesia vanessa (Reinhard), were reared from fi rst collection site (university campus). Th e adults the larvae of M. neustria only from the second emerged between 27 July and 3 August. Although collection site (Tortum). Braconid-killed larvae were Kara and Tschorsnig (2003) listed M. franconica, M. readily recognized by the presence of a parasitoid neustria (Lepidoptera: Lasiocampidae), Euproctis cocoon within the dried skin of the larvae, which chrysorrhoea , and Leucoma salicis (Lepidoptera: was fi rmly attached to the leaves and the twigs. Th e Lymantriidae) as hosts of P. nudioculata, this adult parasitoids emerged about 1 week aft er the parasitoid species proved to be a new record for larvae were killed. Th e adults of M. lionotus emerged the Turkish fauna. Tachina praeceps Meigen was 26-29 July and those of C. vanessa emerged 24-27 reared from the larvae of M. neustria from the fi rst July. Both of these parasitoid species were reared and second collection sites. In some samples, 2-3 from M. neustria for the fi rst time. Operophtera parasitoid larvae developed in 1 host larva. Aft er the brumata; Th era juniperata, T. obeliscata, and T. host died, the parasitoid larvae entered the soil and variata (Lepidoptera: Geometridae); and continued their development into pupae. Th e adults sertifer (Hymenoptera: Diprionidae) were reported emerged 24-27 July and were identifi ed as parasitoids as the hosts of M. lionotus (Yu et al., 2006) . Cotesia of M. neustria (Herting, 1960). Doğanlar (1982b) vanessa presented a larger spectrum of host species;

452 H. ÖZBEK, S. ÇORUH

Yu et al. (2006) listed about 30 species in the and there are many species in various families lepidopteran families including Lasiocampidae, in diff erent orders that serve as primary hosts of Noctuidae, Nolidae, Notodontidae, Nymphalidae, E. urozonus: Apionidae, Attelabidae, Bruchidae, , and . However, M. lionotus Chrysomelidae, Coccinellidae, Curculionidae, was more prevalent than C. vanessa; the fi rst and Scolytidae (Coleoptera); Agromyzidae, accounted for 67% and the second for 33% of the Cecidomyiidae, and Tephritidae (Diptera); braconid species. As the literature records, Kansu et Aphididae, Coccidae, and Diaspididae (Hemiptera); al. (1986) added 2 braconid species, Apanteles sp. and Cynipidae, Diprionidae, Eurytomidae, Pteromalidae, Meteorus sp., from M. neustria in central Anatolia. Tenthredinidae, and (Hymenoptera); Parasitoid species in the Chalcidoidea, 2 Asaphes and Coleophoridae, Gelechiidae, , (Pteromalidae) species, were reared from the larvae Lasiocampidae, Lymantriidae, Pieridae, , of M. neustria collected on the university campus and Yponomeutidae (Lepidoptera) (Natural (fi rst site): A. suspensus (Nees) and A. vulgaris History Museum, 2010). Eurytoma verticillata (F.) Walker. Adults of the fi rst species emerged on 7 July (Eurotomatidae) was recorded in Oltu, the third and those from the second species on 12 July. Both collection site. Th e adults emerged on 16 June. It was species were new parasitoids of M. neustria. Gary et al. fi rst reared from M. neustria. It is known worldwide (1998) indicated that Asaphes was usually considered and is a well-known hyperparasitoid of Lepidoptera an exclusive hyperparasitoid of aphids. Various through Tachinidae, Ichneumonidae, and especially species in the families Agromyzidae, Cecidomyiidae Braconidae (Borlani, 1994). Among its hosts, various (Diptera), and Aphididae (Hemiptera) were primary parasitoids of many species in diff erent recognized as primary hosts of A. suspensus (Natural families in the orders Hemiptera, Lepidoptera, History Museum, 2010). Asaphes vulgaris had more and Hymenoptera were recorded (Natural History primary hosts than A. suspensus. Several curculionid Museum, 2010). Monodontomerus aereus Walker species (Coleoptera); some species in the families (Torymidae) was reared from the larvae of M. neustria Agromyzidae, Cecidomyiidae, Syrphidae (Diptera), collected from Oltu. Th e adults emerged on 11 July. Coccidae, Diaspididae, Pseudococcidae, Aphididae, Doğanlar (1984) obtained it from M. neustria, M. Psyllidae and (Hemiptera); and 1 cynipid species franconica, Euproctis chrysorrhoea L., Leucoma salicis (Hymenoptera: Cynipidae) were indicated as hosts L., and Yponomeuta malinella L. in Erzurum. Kansu of A. suspensus (Natural History Museum, 2010). et al. (1986) obtained it from Aporia crataegi (L.), Brachymeria secundaria (Ruschka) (Chalcididae) Euproctis chrysorrhoea L., M. neustria, and Archips was obtained only in the larvae collected at the third sp. in central Anatolia. Sarıkaya and Avcı (2005) collection site, Oltu. Th e adults emerged 1-3 August. recently obtained M. aereus from Choristoneura It was believed to be a primary parasitoid and the fi rst murinana (Hbn.) (Lepidoptera: Tortricidae). Boucek reared from M. neustria. Several species in diff erent (1970) noted that this species has been recorded families (Geometridae, Lymantriidae, Noctuidae, as a parasite in pupae of many Lepidoptera and in Notodontidae, Nymphalidae, Pieridae, Tortricidae, cocoons of some diprionid sawfl ies. Many primary and Yponomeutidae) in the order Lepidoptera hosts in Hymenoptera and Lepidoptera were were known hosts of this species (Natural History listed (Natural History Museum, 2010). Pediobius Museum, 2010). Eupelmus urozonus Dalman bruchicida Rondani () was reared from (Eupelmidae) was reared from the larvae collected larvae of M. neustria collected from the second at the fi rst collection site, the university campus. Th e collection site, Tortum. Th e adults emerged on 11 adults emerged on 18 July. It was obtained from M. August. Th is was the fi rst time that P. bruchicida neustria for the fi rst time. Eupelmus urozonus was was reared from M. neustria. It was previously found to be one of the primary parasitoids of olive obtained from the larvae of E. chrysorrhoea as a fl y, Dacus oleae Gmelin (Diptera: Tephritidae), and primary parasitoid (Öncüer et al., 1977). However, has received considerable attention in the olive- P. bruchicida was noted as the hyperparasitoid in growing countries of the Mediterranean basin Uraba lugens Walker (Lepidoptera: Nolidae) by Berry (Neuenschwander, 1982; Mustafa and Al-Zaghal, and Mansfi eld (2006) and in Sesamia cretica Led. 1987). It is thought to be exceptionally polyphagous, (Lepidoptera: Noctuidae) by Temerak (2009). Many

453 Larval parasitoids and larval diseases of Malacosoma neustria L. (Lepidoptera: Lasiocampidae) detected in Erzurum Province, Turkey

species in various orders and families were listed emerged 25-27 July. It was reported in Erzurum as hosts of this species (Natural History Museum, Province from faunistic studies conducted by 2010). Pronotalia carlinarum (Szelényi & Erdös) Çoruh and Özbek (2008). Lipara lucens (Diptera: (Eulophidae) was reared from M. neustria collected Chloropidae) was already on record as the host from Tortum. Th e adults emerged 11-13 July. It was of this parasitoid species (Kolarov, 1997). From previously known as a parasitoid of M. neustria the university campus, 2 Gregopimpla species, G. (Natural History Museum, 2010). Other hosts of P. malacosomae (Seyrig) and G. inquisitor (Scopoli), were carlinarum were recorded from various species of recorded. Th e adults of both species emerged almost Diptera in diff erent families, such as Agromyzidae, at the same time (28-30 July). Th e fi rst was already Calliphoridae, and particularly Tephritidae (Natural known as a parasitoid of M. neustria (Th ompson, History Museum, 2010). Psychophagus omnivorus 1957; Kolarov, 1997). Gregopimpl a malacosomae is a (Walker) (Pteromalidae) was reared from M. neustria monophagous species and, currently, M. neustria is collected from Oltu. Th e adults emerged on 29 July. the only known host of this parasitoid species. Th e It was already known as a parasitoid of M. neustria. second species, G. inquisitor, was polyphagous and It attacked M. disstria and M. americanum (L.) parasitized more than 80 species in diff erent orders (Natural History Museum, 2010). It was designated and families such as Curculionidae, Scarabeidae, as a pupal parasitoid of various pest species, such as Arctiidae, Gelechiidae, Geometridae, Gracilariidae, Chrysodeixis chalcites, Spodoptera exigua, Lacanobia Hyponomeutidae, Lycaenidae, Lymantriidae, oleracea (Lepidoptera: Noctuidae) (Mosson et al., Momphididae, Noctuidae, Notodontidae, 1997), and Hyphantria cunea Drury (Lepidoptera: Nymphalidae, Pieridae, Phalaenidae, Phycitidae, Arctiidae) (Rezaei et al., 2003). Additionally, Ips Saturnidae, Sphingidae, Th aumetopoeidae, typographus (L.) (Coleoptera: Scolytidae), several Tortricidae, Zygaenidae, and Tenthredinidae sawfl y species, and many species in various families (Th ompson, 1957; Sedivy, 1963; Townes et al., 1965; of Lepidoptera were listed as hosts of P. omnivorus Shaumar, 1966; Kolarov, 1997). Itoplectis viduata (Natural History Museum, 2010). Only one female Gravenhorst was recorded on the university campus of Torymus triangularis Th omson (Torymidae) was and was already known as a parasitoid of M. neustria. reared on 18 June 2004 from the larvae collected at the Th e adults emerged on 28 July. It attacked various second site, Tortum, and it was a new parasitoid of M. species in lepidopteran families such as Aegeridae, neustria. Among the chalcidoid parasitoids, M. aereu s Gelechiidae, Lymantriidae, Noctuidae, Phalaenidae, and B. secundaria were the most prevalent species Pieridae, Pyralidae, Pyraustidae, Tortricidae, and and accounted for 35.29% and 32.35%, respectively. Zyganidae (Th ompson, 1957; Sedivy, 1965; Aubert, As stated in the literature, Brachymeria intermedia 1969; Kasparyan, 1973; Kolarov, 1997). Lysibia nana (Nees) (Chalcididae) was obtained from the of (Gravenhorst) was reared from the M. neustria larvae M. neustria in central Anatolia by Kansu et al. (1986). collected on the university campus, and it was fi rst Th e present study and published literature revealed reared from M. neustria in the present study. Th e that a total of 11 chalcidoid species were associated adults emerged 24-26 July. Some species in various with the larvae of M. neustria in Turkey. We have to families such as Noctuidae, Pieridae, Notodontidae, admit that we could not precisely detect whether all and Braconidae were known as hosts of this parasitoid chalcidoids were primary parasitoids of M. neustria ; species (Yu et al., 2006). From larvae collected in among them, gregarious and solitary species may Tortum and Oltu, 2 Pimpla species, P. tur i onel l ae L. have occurred. Further studies should be conducted and P. r ufi pes Brulle, were reared from M. neustria. on the chalcidoid parasitoids of M. neustria in Turkey. Th e adults of the fi rst species emerged 20-23 July, and Of the 10 ichneumonid species reared, Exeristes the adults of the second species emerged between 10 roborator F. was the most prevalent and accounted June and 4 July. Pimpla turionellae was recorded as a for 35%. It was recorded from all 3 collection sites. parasitoid of M. neustria by Uğur (1985) in Ankara, Th e adults emerged between 14 June and 12 July. E. who reported that it had over 82 hosts among the roborator was known as a parasitoid of M. neustria lepidopteran species. Scambus nigricans (Th omson) (Yu et al., 2006). Endromopoda phragmitidis Perkins was reared from the larvae of M. neustria collected was found only on the university campus. Th e adults on the university campus. Th e adults emerged 20-23

454 H. ÖZBEK, S. ÇORUH

July. Th is species was already recorded as a parasitoid in place by their midsection, like an inverted V. Th e of M. neustria (Yu et al., 2006). It was known to infected larvae appeared sluggish and turned dark in attack various species in diff erent orders and families color aft er death. (Th ompson, 1957; Kolarov, 1997). Tromatobia Th e second was bacterial; 4 pathogenic bacteria ornata (Gravenhorst) was also collected from the species, Brevibacillus agri, Alcaligenes xylosoxydans university campus. Th e adults emerged 1-4 August. It xylosoxydans (Achromobacter xylosoxidans), Bacillus was previously known as a parasitoid of M. neustria lentimorbus, and Serratia fonticola, were detected (Th ompson, 1957; Kolarov, 1997). Pimpla turionellae in the diseased larvae (Table 2). Among these, was reported from M. neustria in central Anatolia by Brevibacillus agri was isolated from the larvae of M. Kansu et al. (1986) and Pimpla illecebrator (Villers) neustria and an experiment was conducted under was reported in Ankara by Özdemir and Kılınçer fi eld and laboratory conditions (Aslan et al., 2005). (1990); both are parasitoids of M. neustria. Th e Aslan et al. (2005) found that in the laboratory, present study and published literature revealed that during the fi rst 8-h period the mortality was 30% in a total of 11 ichneumonid species parasitized M. both second and third instar larvae, and in fourth neustria larvae in Turkey. Among the ichneumonids, instar larvae it was 10%; under fi eld conditions, the E. roborator was found to be the most common species mortalities at the end of 48 h were 33.3% and 37.5% and accounted for 35%. Th is species was followed by in the third and fourth instar larvae, respectively. No P. tur i onel l ae and P. r ufi pes, each one accounting for experiment was carried out on the other bacteria. 15% of the ichneumonid records. Alcaligenes xylosoxydans was isolated for the fi rst On the basis of the data recorded in the present time from human ear discharge by Yabuuchi and study, it would be reasonable to conclude that Yano (1981). Many benefi cial functions of this parasitoids in general and E. roborator, P. tur i onel l ae , species have been reported in experimental assays, P. r ufi pes, T. praeceps, and P. pavida in particular including control of some plant pathogens (Vaidya et could play a major role in controlling M. neustria in al., 2001), stimulation of ionic transport to promote the fi eld. plant growth (Bertrand et al., 2000), and inhibition of afl atoxin production in Aspergillus sp. (Yan et Disease agents associated with the larvae of M. al., 2004). Moretti et al. (2008) used Achromobacter neustria xylosoxidans (MM1) against Fusarium wilt in During this study, 2 types of diseases were diagnosed tomato under glasshouse conditions and reduced in the larvae of M. neustria. Th e fi rst was NPV, which wilt incidence by about 50%. Bacillus lentimorbus was observed killing larvae in the fi eld. Th e larvae (Paenibacillus lentimorbus) was one of the causative killed by NPV were characteristically found hanging agents of milky disease in Japanese beetle, Popillia

Table 2. Pathogenic bacteria recorded from the larvae of Malacosoma neustria L. in Turkey, including present study.

Name of bacteria Reference

Alcaligenes xylosoxydans xylosoxydans Present study Bacillus lentimorbus Present study Serratia fonticola Present study Brevibacillus agri Present study Bacillus thuringiensis Yaman et al., 2002 Proteus mirabilis Yaman et al., 2002 Staphylococcus sp. Yaman et al., 2002 Pseudomonas chlororaphis Yaman et al., 2002 Pseudomonas sp. Yaman et al., 2002

455 Larval parasitoids and larval diseases of Malacosoma neustria L. (Lepidoptera: Lasiocampidae) detected in Erzurum Province, Turkey

japonica Newman (Coleoptera: Scarabaeidae), and species, pirarucu (Arapaima gigas). Our study is the related scarab larvae (Rippere et al., 1998). Serratia fi rst report that S. fonticola was isolated from insect fonticola was described as a new species of the larva of M. neustria. Of course, further studies will be Serratia from fresh water and soil by Gavini et al. required to confi rm this. (1979). It has since been related to contaminants in the respiratory tract and has been isolated in the As recorded in the literature, Yaman et al. (2002) droppings of European wild birds (Muller et al., isolated Bacillus thuringiensis, Proteus mirabilis, 1986). It is a bacte rium with an extensive distribution Staphylococcus sp., Pseudomonas chlororaphis, and in aquatic environments (Farmer et al., 1985). It was Pseudomonas sp. from M. neustria and found that B. recogn ized to be a human pathogen in the beginning thuringiensis, Proteus mirabilis, and P. chlororaphis of the 1990s (Bollet et al., 1991). Recently, Casiano showed infection of the fi rst and second instar larvae et al. (2008) isolated this bacterium from a fi sh of M. neustria (Table 3).

Table 3. Parasitoids of Malacosoma neustria L. recorded in Turkey, including present study.

Name of parasitoid Order and family Stage of the host Reference(s) Baryscapus nigroviolaceus Hym.: Eulophidae Egg Özbek and Çoruh, 2010 Baryscapus oophagus Hym.: Eulophidae Egg Özbek and Çoruh, 2010 Baryscapus evonymella Hym.: Eulophidae Egg Özbek and Çoruh, 2010 Pronotalia carlinarum Hym.: Eulophidae Egg Özbek and Çoruh, 2010 Trichogramma buluti Hym.: Egg Bulut, 1991; Özbek and Çoruh, 2010 Anastatus bifasciatus Hym.: Trichogrammatidae Egg Bulut, 1991; Özbek and Çoruh, 2010 Telenomus laevisculus Hym.: Scelionidae Egg Bulut, 1991; Özbek and Çoruh, 2010 Ooencyrtus neustriae Hym.: Egg Bulut, 1991; Özbek and Çoruh, 2010 Ooencyrtus tardus Hym.: Encyrtidae Egg Bulut, 1991 Ooencyrtus masii Hym.: Encyrtidae Egg Bulut, 1991 Ooencyrtus sp. Hym.: Encyrtidae Egg Bulut, 1991 Drino inconspicua Dip.: Tachinidae Larva Doğanlar, 1975 Drino imberbis Dip.: Tachinidae Larva Doğanlar, 1975 Exorista amoena Dip.: Tachinidae Larva Present study E. larvarum Dip.: Tachinidae Larva Kara and Tschorsnig, 2003; present study E. segregate Dip.: Tachinidae Larva Kara and Tschorsnig, 2003; present study Compsilura concinnata Dip.: Tachinidae Larva Kansu et al., 1986 Masicera sphingivora Dip.: Tachinidae Larva Kara and Tschorsnig, 2003; present study Pales pavida Dip.: Tachinidae Larva Present study Palesisa nudioculata Dip.: Tachinidae Larva Present study Tachina praeceps Dip.: Tachinidae Larva Present study Apanteles sp. Hym.: Braconidae Larva Kansu et al., 1986 Meteorus sp. Hym.: Braconidae Larva Kansu et al., 1986 Meteorus lionotus Hym.: Braconidae Larva Present study Cotesia Vanessa Hym.: Braconidae Larva Present study Asaphes suspensus Hym.: Pteromalidae Larva Present study A. vulgaris Hym.: Pteromalidae Larva Present study Psychophagus omnivorus Hym.: Pteromalidae Larva Present study Brachymeria secundaria Hym.: Chalcididae Larva Present study Eupelmus urozonus Hym.: Eupelmidae Larva Present study Eurytoma verticillata Hym.: Eurotomatidae Larva Present study Pediobius bruchicida Hym.: Eulophidae Larva Present study Pronotalia carlinarum Hym.: Eulophidae Larva Present study Monodontomerus aereus Hym.: Torymidae Pupa Doğanlar, 1984; Kansu et al., 1986; present study Torymus triangularis Hym.: Torymidae Larva Present study Endromopoda phragmitidis Hym.: Ichneumonidae Larva Çoruh and Özbek, 2008; present study Exeristes roborator Hym.: Ichneumonidae Larva Present study Gregopimpla inquisitor Hym.: Ichneumonidae Larva Present study G. malacosomae Hym.: Ichneumonidae Larva Present study Itoplectis viduata Hym.: Ichneumonidae Larva Present study Lysibia nana Hym.: Ichneumonidae Larva Present study Pimpla illecebrator Hym.: Ichneumonidae Pupa Özdemir and Kılınçer, 1990 Pimpla turionellae Hym.: Ichneumonidae Pupa Uğur, 1985; Kansu et al., 1986; present study P. r ufi pes Hym.: Ichneumonidae Larva Present study Scambus nigricans Hym.: Ichneumonidae Larva Present study Tromatobia ornata Hym.: Ichneumonidae Larva Present study

456 H. ÖZBEK, S. ÇORUH

Conclusion high as they are also suggested to be very important Th e data presented here revealed that larval parasitoids natural control agents in the fi eld. Th us, by taking could play an important role in controlling M. into consideration all of the natural enemies of M. neustria in Erzurum Province as the parasitism rate neustria, it can be emphasized that pest control was high (33.7%). Additionally, Özbek and Çoruh strategies should address the preservation of these (2010) determined egg parasitoids of M. neustria and other natural enemies via judicious use of in Erzurum, and the parasitism rate was 21.81%. As pesticides that have a minimal impact on the natural disease agents, NPV and pathogenic bacteria were enemy’s complex. In addition, where possible, other biological agents involved in the regulation of suitable habitats should be provided in and around the outbreaks of M. neustria in Erzurum Province. fi elds to encourage the development and survival of Furthermore, all of the natural enemies of M. neustria natural enemies. recor ded so far in Turkey are listed in Table 3. As a whole, these organisms, in addition to atmospheric Acknowledgments conditions, must have regulated the population of M. neustria under natural conditions in Turkey. Th e authors are thankful to Dr M. Doğanlar Witter et al. (1972) noted that weather conditions, (Chalcidoidea), Dr J. Kolarov (Ichneumonidae), starvation, parasitoids, diseases, and genetic factors, Dr A. Beyarslan (Braconidae), and Dr K. Kara either separately or together, were responsible in the (Tachinidae) for identifi cation of the parasitoids. collapse of M. disstria Hubner outbreaks. It should We are also thankful to Dr Fikrettin Şahin and Dr be noted that all of the parasitoids recorded as larval Arzu Ala Görmez for isolation and determination parasitoids of M. neustria in the present study were of bacteria. Th e fi rst author (H.Ö.) extends his polyphagous, except Gregopimpla malacosomae. appreciation to Dr Yamuna D. Pande for carefully Th eir potential, especially that of the latter species, as reading the manuscript and off ering linguistic candidates for biological control agents of this pest is suggestions.

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